Skip to main content
Log in

Regulation of omega-3 fatty acids production by different genes in freshwater fish species: a review

  • Review
  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

The present study aims to compare the gene expression of three different fish species (common carp, tilapia, and trout) with varying levels of fatty acids (FA). Based on transcriptome analysis and RNA sequencing, various genes and their associated metabolic pathways are identified. Pathways are categorized based on the genes they encode. Genes that were differentially expressed and their promoter’s methylation patterns were revealed by RNA-seq analysis in common carp. Furthermore, fatty acid–enriched pathways, such as ARA4 and adipocytokine signaling, were also identified. Many genes and pathways may influence tilapia’s growth and omega-3 content. Using the mTOR pathway, trout with differential expression were discovered to be involved in producing omega-3 fatty acids. This study revealed major pathways in fish species to produce omega-3 fatty acids.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Data Availability

Not applicable.

Abbreviations

FAs:

Fatty acids

DHA:

Docosahexaenoic acid

EPA:

Eicosapentanoic acid

ALA:

Alpha-linolenic acid

PUFAs:

Polyunsaturated fatty acids

RNA-seq:

RNA sequencing

NGS:

Next-generation sequencing

QTL:

Quantitative trait locus

DEGs:

Differentially expressed genes

DMRs:

Differentially methylated regions

DET:

Differentially expressed transcripts

GO:

Gene Ontology

Val:

Valine

Leu:

Leucine

Ile:

Isoleucine

qPCR:

Quantitative polymerase chain reaction

FADS1:

Fatty acid desaturase 1

FADS2:

Fatty acid desaturase 2

References

  • Agaba M, Tocher DR, Dickson CA, Dick JR, Teale AJ (2004) Zebrafish cDNA encoding multifunctional fatty acid elongase involved in production of eicosapentaenoic (20: 5n-3) and docosahexaenoic (22: 6n-3) acids. Mar Biotechnol 6(3):251–261

    Article  CAS  Google Scholar 

  • Anton-Pardo M, Adamek Z (2015) The role of zooplankton as food in carp pond farming: a review. J Appl Ichthyol 31:7–14

    Article  Google Scholar 

  • Arts MT, Kohler CC (2009) Health and condition in fish: the influence of lipids on membrane competency and immune response. Lipids in Aquatic Ecosystems 237–256

  • Bohm M, Schultz S, Koussoroplis AM, Kainz MJ (2014) Tissue-specific fatty acids response to different diets in common carp (Cyprinus carpio L.). PLoS One 9(4):e94759

    Article  PubMed  PubMed Central  Google Scholar 

  • Bostock J, McAndrew B, Richards R, Jauncey K, Telfer T, Lorenzen K, Corner R (2010) Aquaculture: global status and trends. Philos Trans R Soc Lond, B, Biol Sci 365(1554):2897–2912

    Article  PubMed  Google Scholar 

  • Bowman TA, O'Keeffe KR, D'Aquila T, Yan QW, Griffin JD, Killion EA, Greenberg AS (2016) Acyl CoA synthetase 5 (ACSL5) ablations in mice increases energy expenditure and insulin sensitivity and delays fat absorption. Mol Metab 5(3):210–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calder PC (2018) Very long-chain n-3 fatty acids and human health: fact, fiction and the future. Proc Nutr Soc 77(1):52–72

    Article  CAS  PubMed  Google Scholar 

  • Castro LFC, Tocher DR, Monroig O (2016) Long-chain polyunsaturated fatty acid biosynthesis in chordates: insights into the evolution of Fads and Elovl gene repertoire. Prog Lipid Res 62:25–40

    Article  CAS  PubMed  Google Scholar 

  • Chang YS, Tsai CT, Huangfu CA, Huang WY, Lei HY, Lin CF, Lai MD (2011) ACSL3 and GSK-3β are essential for lipid upregulation induced by endoplasmic reticulum stress in liver cells. J Cell Biochem 112(3):881–893

    Article  CAS  PubMed  Google Scholar 

  • Collins FS (1995) Positional cloning moves from perditional to traditional. Nat Genet 9(4):347–350

    Article  CAS  PubMed  Google Scholar 

  • Dai W, Panserat S, Plagnes-Juan E, Seiliez I, Skiba-Cassy S (2015) Amino acids attenuate insulin action on gluconeogenesis and promote fatty acid biosynthesis via mTORC1 signaling pathway in trout hepatocytes. Cell Physiol Biochem 36(3):1084–1100

    Article  CAS  PubMed  Google Scholar 

  • Dentin R, Denechaud PD, Benhamed F, Girard J, Postic C (2006) Hepatic gene regulation by glucose and polyunsaturated fatty acids: a role for ChREBP. J Nutr 136(5):1145–1149

    Article  CAS  PubMed  Google Scholar 

  • Fehlinger L, Mathieu-Resuge M, Pilecky M, Parmar TP, Twining CW, Martin-Creuzburg D, Kainz MJ (2023) Export of dietary lipids via emergent insects from eutrophic fishponds. Hydrobiologia 850(15):3241–3256

    Article  CAS  PubMed  Google Scholar 

  • Geay F, Wenon D, Mellery J, Tinti E, Mandiki SN, Tocher DR, Kestemont P (2015) Dietary linseed oil reduces growth while differentially impacting LC-PUFA synthesis and accretion into tissues in Eurasian perch (Perca fluviatilis). Lipids 50(12):1219–1232

    Article  CAS  PubMed  Google Scholar 

  • Guo H, Gu W, Sun P, Bai Q, Wang B (2016) Transcriptome analyses reveal lipid metabolic process in liver related to the difference of carcass fat content in rainbow trout (Oncorhynchus mykiss). International Journal of Genomics 2016:1–10. https://doi.org/10.1155/2016/7281585

    Article  CAS  Google Scholar 

  • Gutiérrez J, Åsgård T, Fabbri E, Plisetskaya EM (1991) Insulin-receptor binding in skeletal muscle of trout. Fish Physiol Biochem 9(4):351–360

    Article  PubMed  Google Scholar 

  • Han F, Song Q, Zhang Y, Wang X, Wang Z (2017) Molecular characterization and immune responses of Rab5 in large yellow croaker (Larimichthys crocea). Aquac Fish 2(4):165–172

    Article  Google Scholar 

  • Henriques J, Dick JR, Tocher DR, Bell JG (2014) Nutritional quality of salmon products available from major retailers in the UK: content and composition of n-3 long-chain PUFA. Br J Nutr 112(6):964–975

    Article  CAS  PubMed  Google Scholar 

  • Ivanova A, Hadzhinikolova L (2015) Evaluation of nutritional quality of common carp (Cyprinus carpio L.) lipids through fatty acid ratios and lipid indices. Bulg J Agric Sci 21:180–185

    Google Scholar 

  • Jakobsson A, Westerberg R, Jacobsson A (2006) Fatty acid elongases in mammals: their regulation and roles in metabolism. Prog Lipid Res 45(3):237–249

    Article  CAS  PubMed  Google Scholar 

  • Jiang Y, Zhang S, Xu J, Feng J, Mahboob S, Al-Ghanim KA, Xu P (2014) Comparative transcriptome analysis reveals the genetic basis of skin color variation in common carp. PLoS One 9(9):e108200

    Article  PubMed  PubMed Central  Google Scholar 

  • Joseph R, Poschmann J, Sukarieh R, Too PG, Julien SG, Xu F, Stunkel W (2015) ACSL1 is associated with fetal programming of insulin sensitivity and cellular lipid content. Mol Endocrinol 29(6):909–920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kainz M, Arts MT, Mazumder A (2004) Essential fatty acids in the planktonic food web and their ecological role for higher trophic levels. Limnol Oceanogr 49(5):1784–1793

    Article  CAS  Google Scholar 

  • Kainz M, Brett MT, Arts MT (eds) (2009) Lipids in aquatic ecosystems. Springer-Verlag, New York

    Google Scholar 

  • Khan AHPJ, Pessin J (2002) Insulin regulation of glucose uptake: a complex interplay of intracellular signaling pathways. Diabetologia 45(11):1475–1483

    Article  CAS  PubMed  Google Scholar 

  • Kolditz CI, Paboeuf G, Borthaire M, Esguerra D, San Cristobal M, Lefevre F, Médale F (2008) Changes induced by dietary energy intake and divergent selection for muscle fat content in rainbow trout (Oncorhynchus mykiss), assessed by transcriptome and proteome analysis of the liver. BMC Genomics 9(1):1–16

    Article  Google Scholar 

  • Laplante M, Sabatini DM (2009) mTOR signaling at a glance. J Cell Sci 122(20):3589–3594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leaver MJ, Bautista JM, Björnsson BT, Jönsson E, Krey G, Tocher DR, Torstensen BE (2008) Towards fish lipid nutrigenomics: current state and prospects for fin-fish aquaculture. Rev Fish Sci 16(sup1):73–94

    Article  CAS  Google Scholar 

  • Levin E, Yom-Tov Y, Hefetz A, Kronfeld-Schor N (2013) Changes in diet, body mass and fatty acid composition during pre-hibernation in a subtropical bat in relation to NPY and AgRP expression. J Comp Physiol B 183(1):157–166

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Monroig O, Zhang L, Wang S, Zheng X, Dick JR, Tocher DR (2010) Vertebrate fatty acyl desaturase with Δ4 activity. Proc Natl Acad Sci 107(39):16840–16845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin G, Chua E, Orban L, Yue GH (2016) Mapping QTL for sex and growth traits in salt-tolerant tilapia (Oreochromis spp. XO. mossambicus). PLoS One 11(11):e0166723

    Article  PubMed  PubMed Central  Google Scholar 

  • Lin G, Thevasagayam NM, Wan ZY, Ye BQ, Yue GH (2019) Transcriptome analysis identified genes for growth and omega-3/-6 ratio in saline tilapia. Front Genet 10:244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin G, Wang L, Ngoh ST, Ji L, Orban L, Yue GH (2018) Mapping QTL for omega-3 content in hybrid saline tilapia. Mar Biotechnol 20(1):10–19

    Article  CAS  Google Scholar 

  • Liu F, Sun F, Li J, Xia JH, Lin G, Tu RJ, Yue GH (2013) A microsatellite-based linkage map of salt tolerant tilapia (Oreochromis mossambicus x Oreochromis spp.) and mapping of sex-determining loci. BMC Genom 14(1):1–14

    Article  CAS  Google Scholar 

  • Liu F, Sun F, Xia JH, Li J, Fu GH, Lin G, Yue GH (2014) A genome scan revealed significant associations of growth traits with a major QTL and GHR2 in tilapia. Sci Rep 4(1):1–9

    Article  Google Scholar 

  • Mathiesen ÁM (2015) The state of world fisheries and aquaculture 2012. FAO Fisheries and Aquaculture Department, Rome, p 230

    Google Scholar 

  • Monroig O, Rotllant J, Cerdá-Reverter JM, Dick JR, Figueras A, Tocher DR (2010) Expression and role of Elovl4 elongases in biosynthesis of very long-chain fatty acids during zebrafish Danio rerio early embryonic development. Biochim Biophys Acta Mol Cell Biol Lipids 1801(10):1145–1154

    Article  CAS  Google Scholar 

  • Monroig Ó, Shu-Chien AC, Kabeya N, Tocher DR, Castro LFC (2022) Desaturases and elongases involved in long-chain polyunsaturated fatty acid biosynthesis in aquatic animals: from genes to functions. Prog Lipid Res 86:101157. https://doi.org/10.1016/j.plipres.2022.101157

  • Monroig O, Wang S, Zhang L, You C, Tocher DR, Li Y (2012) Elongation of long-chain fatty acids in rabbitfish Siganus canaliculatus: cloning, functional characterisation and tissue distribution of Elovl5-and Elovl4-like elongases. Aquaculture 350:63–70

    Article  Google Scholar 

  • Morais S, Monroig O, Zheng X, Leaver MJ, Tocher DR (2009) Highly unsaturated fatty acid synthesis in Atlantic salmon: characterization of ELOVL5-and ELOVL2-like elongases. Mar Biotechnol 11(5):627–639

    Article  CAS  Google Scholar 

  • Nakamura MT, Cheon Y, Li Y, Nara TY (2004) Mechanisms of regulation of gene expression by fatty acids. Lipids 39(11):1077–1083

    Article  CAS  PubMed  Google Scholar 

  • Oboh A, Kabeya N, Carmona-Antonanzas G, Castro LFC, Dick JR, Tocher DR, Monroig O (2017) Two alternative pathways for docosahexaenoic acid (DHA, 22: 6n-3) biosynthesis are widespread among teleost fish. Sci Rep 7(1):1–10

    Article  CAS  Google Scholar 

  • Parrizas MARCELINA, Planas J, Plisetskaya EM, Gutierrez J (1994) Insulin binding and receptor tyrosine kinase activity in skeletal muscle of carnivorous and omnivorous fish. Am J Phys Regul Integr Comp Phys 266(6):R1944–R1950

    CAS  Google Scholar 

  • Pepino MY, Kuda O, Samovski D, Abumrad NA (2014) Structure-function of CD36 and importance of fatty acid signal transduction in fat metabolism. Annu Rev Nutr 34:281–303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plagnes-Juan E, Lansard M, Seiliez I, Medale F, Corraze G, Kaushik S, Skiba-Cassy S (2008) Insulin regulates the expression of several metabolism-related genes in the liver and primary hepatocytes of rainbow trout (Oncorhynchus mykiss). J Exp Biol 211(15):2510–2518

    Article  CAS  PubMed  Google Scholar 

  • Porstmann T, Santos CR, Griffiths B, Cully M, Wu M, Leevers S, Schulze A (2008) SREBP activity is regulated by mTORC1 and contributes to Akt-dependent cell growth. Cell Metab 8(3):224–236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qian X, Ba Y, Zhuang Q, Zhong G (2014) RNA-Seq technology and its application in fish transcriptomics. OMICS: J Integr Biol 18(2):98–110

    Article  CAS  Google Scholar 

  • Ralston JC, Matravadia S, Gaudio N, Holloway GP, Mutch DM (2015) Polyunsaturated fatty acid regulation of adipocyte FADS1 and FADS2 expression and function. Obesity 23(4):725–728

    Article  CAS  PubMed  Google Scholar 

  • Ros-Freixedes R, Gol S, Pena RN, Tor M, Ibáñez-Escriche N, Dekkers JC, Estany J (2016) Genome-wide association study singles out SCD and LEPR as the two main loci influencing intramuscular fat content and fatty acid composition in Duroc pigs. PLoS One 11(3):e0152496

    Article  PubMed  PubMed Central  Google Scholar 

  • Roy J, Larroquet L, Surget A, Lanuque A, Sandres F, Terrier F, Skiba-Cassy S (2020a) Impact on cerebral function in rainbow trout fed with plant-based omega-3 long-chain polyunsaturated fatty acids enriched with DHA and EPA. Fish Shellfish Immunol 103:409–420

    Article  CAS  PubMed  Google Scholar 

  • Roy K, Vrba J, Kaushik SJ, Mraz J (2020b) Feed-based common carp farming and eutrophication: is there a reason for concern. Rev Aquac 12(3):1736–1758

    Article  Google Scholar 

  • Rymer C, Givens DI (2005) n− 3 fatty acid enrichment of edible tissue of poultry: A review. Lipids 40(2):121–130

    Article  CAS  PubMed  Google Scholar 

  • Salin K, Mathieu-Resuge M, Graziano N, Dubillot E, Le Grand F, Soudant P, Vagner M (2021) The relationship between membrane fatty acid content and mitochondrial efficiency differs within-and between-omega-3 dietary treatments. Mar Environ Res 163:105205

    Article  CAS  PubMed  Google Scholar 

  • Santigosa E, Constant D, Prudence D, Wahli T, Verlhac-Trichet V (2020) A novel marine algal oil containing both EPA and DHA is an effective source of omega-3 fatty acids for rainbow trout (Oncorhynchus mykiss). J World Aquacult Soc 51(3):649–665

    Article  CAS  Google Scholar 

  • Sargent J, Bell G, McEvoy L, Tocher D, Estevez A (1999) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177(1–4):191–199

    Article  CAS  Google Scholar 

  • Schultz S, Koussoroplis AM, Changizi-Magrhoor Z, Watzke J, Kainz MJ (2015) Fish oil–based finishing diets strongly increase long-chain polyunsaturated fatty acid concentrations in farm-raised common carp (Cyprinus carpio L.). Aquac Res 46(9):2174–2184

    Article  CAS  Google Scholar 

  • Schuster SC (2008) Next-generation sequencing transforms today’s biology. Nat Methods 5(1):16–18

    Article  CAS  PubMed  Google Scholar 

  • Skiba-Cassy S, Lansard M, Panserat S, Médale F (2009) Rainbow trout genetically selected for greater muscle fat content display increased activation of liver TOR signaling and lipogenic gene expression. Am J Phys Regul Integr Comp Phys 297(5):R1421–R1429

    CAS  Google Scholar 

  • Smathers RL, Petersen DR (2011) The human fatty acid-binding protein family: evolutionary divergences and functions. Hum Genomics 5(3):1–22

    Article  Google Scholar 

  • Srivastava AK, Pandey SK (1998) Potential mechanism (s) involved in the regulation of glycogen synthesis by insulin. Mol Cell Biochem 182(1):135–141

    Article  CAS  PubMed  Google Scholar 

  • Stancheva M, Merdzhanova A (2011) Fatty acid composition of common carp, rainbow trout, and grey mullet fish species. Agric Sci Technol 3(3):285–289

    Google Scholar 

  • Stoneham TR, Kuhn DD, Taylor DP, Neilson AP, Smith SA, Gatlin DM, O’Keefe SF (2018) Production of omega-3 enriched tilapia through the dietary use of algae meal or fish oil: Improved nutrient value of fillet and offal. PLoS One 13(4):e0194241

    Article  PubMed  PubMed Central  Google Scholar 

  • Tocher DR, Betancor MB, Sprague M, Olsen RE, Napier JA (2019) Omega-3 long-chain polyunsaturated fatty acids, EPA and DHA: bridging the gap between supply and demand. Nutrients 11(1):89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tremblay F, Lavigne C, Jacques H, Marette A (2007) Role of dietary proteins and amino acids in the pathogenesis of insulin resistance. Annu Rev Nutr 27:293–310

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Wachholtz M, Wang J, Liao X, Lu G (2014a) Analysis of the skin transcriptome in two oujiang color varieties of common carp. PLoS One 9(3):e90074

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang C, Zhang Z, Yao H, Zhao F, Wang L, Wang X, Xu S (2014b) Effects of atrazine and chlorpyrifos on DNA methylation in the liver, kidney and gill of the common carp (Cyprinus carpio L.). Ecotoxicol Environ Saf 108:142–151

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Wang J, Wang G, Wu C, Li J (2017) Molecular cloning, sequencing, and expression profiles of heat shock protein 90 (HSP90) in Hyriopsis cumingii exposed to different stressors: temperature, cadmium and Aeromonas hydrophila. Aquac Fish 2(2):59–66

    Article  Google Scholar 

  • Wang Y, Wu C, Guo P, Wang G, Li J (2018) Molecular characterization and expression of the feminization-1c (fem-1c) in the freshwater mussel (Hyriopsis cumingii). Aquac Fish 3(1):6–13

    Article  Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10(1):57–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Webster CD, Lim C (eds) (2006) Tilapia: biology, culture, and nutrition. CRC Press

    Google Scholar 

  • Wei K, Niu D, Peng M, Xie S, Wang S, Li J (2018) Characterization of two splice variants of EGFR and their effects on the growth of the razor clam. Aquac Fish 3(2):62–71

    Article  Google Scholar 

  • Wood JD, Enser M, Fisher AV, Nute GR, Sheard PR, Richardson RI, Whittington FM (2008) Fat deposition, fatty acid composition and meat quality: A review. Meat Sci 78(4):343–358

    Article  CAS  PubMed  Google Scholar 

  • Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124(3):471–484

    Article  CAS  PubMed  Google Scholar 

  • Young K (2009) Omega-6 (n-6) and omega-3 (n-3) fatty acids in tilapia and human health: a review. Int J Food Sci Nutr 60(sup5):203–211

    Article  CAS  PubMed  Google Scholar 

  • Yu FX, Guan KL (2013) The Hippo pathway: regulators and regulations. Genes Dev 27(4):355–371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yue GH (2014) Recent advances of genome mapping and marker-assisted selection in aquaculture. Fish Fish 15(3):376–396

    Article  Google Scholar 

  • Zavorka L, Crespel A, Dawson NJ, Papatheodoulou M, Killen SS, Kainz MJ (2021) Climate change-induced deprivation of dietary essential fatty acids can reduce growth and mitochondrial efficiency of wild juvenile salmon. Funct Ecol 35(9):1960–1971

    Article  Google Scholar 

  • Zhang H, Xu P, Jiang Y, Zhao Z, Feng J, Tai R, Xu J (2019) Genomic, transcriptomic, and epigenomic features differentiate genes that are relevant for muscular polyunsaturated fatty acids in the common carp. Front Genet 10:217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao B, Tumaneng K, Guan KL (2011) The Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal. Nat Cell Biol 13(8):877–883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng X, Kuang Y, Lv W, Cao D, Sun Z, Sun X (2016) Genome-wide association study for muscle fat content and abdominal fat traits in common carp (Cyprinus carpio). PLoS One 11(12):e0169127

    Article  PubMed  PubMed Central  Google Scholar 

  • Zheng X, Seiliez I, Hastings N, Tocher DR, Panserat S, Dickson CA, Teale AJ (2004) Characterization and comparison of fatty acyl Δ6 desaturase cDNAs from freshwater and marine teleost fish species. Comp Biochem Physiol B: Biochem Mol Biol 139(2):269–279

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors duly acknowledge Department of Animal Sciences, Central University of Himachal Pradesh for providing facilities to carry out the work.

Author information

Authors and Affiliations

Authors

Contributions

RK - conceptualization; SB and KT - original draft preparation; DS and AKS - reviewing and editing; BB, DM, and SK - helped to draft the final manuscript; all authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Rakesh Kumar.

Ethics declarations

Ethical approval

Not applicable.

Consent to participate

Taken.

Consent for publication

Yes.

Competing interests

The authors declare no completing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bhardwaj, S., Thakur, K., Sharma, A.K. et al. Regulation of omega-3 fatty acids production by different genes in freshwater fish species: a review. Fish Physiol Biochem 49, 1005–1016 (2023). https://doi.org/10.1007/s10695-023-01236-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-023-01236-y

Keywords

Navigation